Beetles Conquered Earth by Evolving Their Own Biochemical Laboratory

Amazing stuff!

"Beetles are the poster child of evolutionary success: about 400,000 species are known—about a quarter of all described lifeforms—and potentially hundreds of thousands more await discovery. The beauty and diversity of beetles enchanted a young Charles Darwin and were the teenage fascination of Alfred Russell Wallace, the co-discoverers of evolution by natural selection. ...
the rove beetles (Staphylinidae) a sprawling radiation of over 66,000 species—not just the largest beetle family, but the largest family in the entire animal kingdom. Rove beetles are an enigma: they seem to have both forsaken strongly protective elytra [the hardened shield-like structures that protect the flight wings] and are mostly predatory instead of feeding on plants. Yet, they exploded across Earth's biosphere, invading every terrestrial niche imaginable over the past 200 million years. ...

evolution of two cell types that form a chemical defense gland within these beetles' bodies as a catalyst behind their global radiation.

In 2021, researchers in the Parker lab studied a gland in rove beetles called the "tergal gland," a structure at the tip of their flexible abdomens. The team showed how the tergal gland is made up of two unique cell types: one that makes toxic compounds called benzoquinones, and another that makes a liquid mixture (or solvent) into which the benzoquinones dissolve, creating a potent cocktail that the beetle discharges at predators. ...

In the new work ... assembled whole genomes from a diverse set of species spanning the rove beetle evolutionary tree, and analyzed the genes expressed with the gland's two cell types. Doing so enabled them to uncover an ancient genetic toolkit that evolved over 100 million years ago, equipping these insects with their powerful chemical defenses.

"... how similar the genetic architecture of the gland was across this massive group of beetles,"  ... "It was when we started to look at specific gene families, we found hundreds of ancient genes that had found new functions within the gland, and a small but essential set of evolutionarily new genes. These new genes were key to rove beetles evolving their amazing chemistry.  ...

Retracing the molecular steps in gland evolution, the team identified a major evolutionary innovation in the way the beetles evolved to safely manufacture the poisonous benzoquinones. They found that rove beetles hit upon a mechanism of toxin secretion that is strikingly similar to how plants control the release of chemical compounds that deter herbivores. They bind the toxin to a sugar molecule, rendering it inactive, and then cleave the toxin from the sugar only when the chemical is secreted safely outside of the beetle's own cells. ...

This mechanism evolved in the Early Cretaceous; after they evolved it, the beetles started to radiate into tens or possibly hundreds of thousands of species. "It's the archetypal key innovation. Once they hit upon this solution, it really took them places, evolutionarily-speaking," ... Related rove beetle lineages that lack the gland have not had the same evolutionary diversification, numbering only tens to hundreds of species.

By exploring the chemistries of different species, the researchers found that, remarkably, while the two cell types comprising the gland have stayed largely the same, the chemicals they produce can evolve dramatically, adapting rove beetles to different ecological niches. The gland can be thought of as a kind of chemical laboratory in which a beetle species can synthesize the compounds needed to live in new environments. For example, one group of rove beetles evolved to prey on mites and repurposed the gland to secrete mite sex pheromones; another lives inside ant colonies, and produces chemicals that pacify the otherwise highly aggressive worker ants, enabling the beetle to live symbiotically with the ants, and even prey upon them. ..."

From the highlights and abstract:

"Highlights

• Two novel cell types form the rove beetle tergal gland, a key evolutionary innovation

• Cellular mechanisms of biosynthesis revealed, encoded by ancient expression programs

• Reprogramming biosynthesis yielded new compounds underlying ecological specialization

• The tergal gland exemplifies cell type innovation driving macroevolutionary success

Summary

How evolution at the cellular level potentiates macroevolutionary change is central to understanding biological diversification. The >66,000 rove beetle species (Staphylinidae) form the largest metazoan family. Combining genomic and cell type transcriptomic insights spanning the largest clade, Aleocharinae, we retrace evolution of two cell types comprising a defensive gland—a putative catalyst behind staphylinid megadiversity. We identify molecular evolutionary steps leading to benzoquinone production by one cell type via a mechanism convergent with plant toxin release systems, and synthesis by the second cell type of a solvent that weaponizes the total secretion. This cooperative system has been conserved since the Early Cretaceous as Aleocharinae radiated into tens of thousands of lineages. Reprogramming each cell type yielded biochemical novelties enabling ecological specialization—most dramatically in symbionts that infiltrate social insect colonies via host-manipulating secretions. Our findings uncover cell type evolutionary processes underlying the origin and evolvability of a beetle chemical innovation."

Beetles Conquered Earth by Evolving Their Own Biochemical Laboratory - www.caltech.edu As organisms diversified on planet Earth, some branches of the tree of life became exceptionally diverse, others far less so. Still others went extinct. Why evolution favored certain groups over others is a long-standing question in evolutionary science.

The genomic and cellular basis of biosynthetic innovation in rove beetles (no public access)

Graphical abstract